Journal of Ecology. 2019;107:2121–2132. wileyonlinelibrary.com/journal/jec  | 2121© 2019 The Authors. Journal of Ecology © 2019 British Ecological Society

Received:25January2019  |  Accepted:3May2019DOI: 10.1111/1365-2745.13253

I S P H Y L O G E N E T I C A N D F U N C T I O N A L T R A I T D I V E R S I T Y A D R I V E R O R C O N S E Q U E N C E O F G R A S S L A N D C O M M U N I T Y A S S E M B LY ?

Resource addition drives taxonomic divergence and phylogenetic convergence of plant communities

Xian Yang1  | Guoyong Li2  | Shaopeng Li3,4 | Qianna Xu1 | Pandeng Wang5 | Huanhuan Song2 | Danyu Sun2 | Mingxing Zhong2  | Zhenxing Zhou2 | Jian Song6  | Jingyi Ru2 | Shiqiang Wan6 | Lin Jiang1

1SchoolofBiologicalSciences,GeorgiaInstituteofTechnology,Atlanta,Georgia,USA;2StateKeyLaboratoryofCottonBiology,KeyLaboratoryofPlantStressBiology,CollegeofLifeSciences,HenanUniversity,Kaifeng,China;3ZhejiangTiantongForestEcosystemNationalObservationandResearchStation,SchoolofEcologicalandEnvironmentalSciences,EastChinaNormalUniversity,Shanghai,China;4InstituteofEco‐Chongming(IEC),Shanghai,China;5StateKeyLaboratoryofBiocontrol,GuangdongKeyLaboratoryofPlantResources,SchoolofLifeSciences,SunYat‐senUniversity,Guangzhou,Chinaand6CollegeofLifeSciences,HebeiUniversity,Baoding,China

CorrespondenceShiqiang WanEmail:swan@hbu.edu.cn

LinJiangEmail:lin.jiang@biology.gatech.edu

Funding informationNationalNaturalScienceFoundationofChina,Grant/AwardNumber:31361123001,31430015and31770522;NationalScienceFoundation,Grant/AwardNumber:DEB‐1342754,DEB‐1856318andCBET‐1833988

HandlingEditor:DavidGibson

Abstract1. Anthropogenic environmental changes are known to affect theEarth's ecosys-tems. However, how these changes influence assembly trajectories of the im-pactedcommunitiesremainsalargelyopenquestion.

2. Inthisstudy,weinvestigatedtheeffectofelevatednitrogen(N)depositionandin-creasedprecipitationonplanttaxonomicandphylogeneticβ‐diversityina9‐yearfieldexperimentinthetemperatesemi‐aridsteppeofInnerMongolia,China.

3. WefoundthatbothNandwateradditionsignificantlyincreasedtaxonomicβ-di-versity,whereasN,notwater,additionsignificantlyincreasedphylogeneticβ-di-versity.Afterthedifferencesinlocalspeciesdiversitywerecontrolledusingnullmodels,thestandardeffectsizeoftaxonomicβ‐diversitystillincreasedwithbothNandwateraddition,whereaswater,notN,addition,significantlyreducedthestandardeffectsizeofphylogeneticβ‐diversity.Theincreasedphylogeneticcon-vergenceobservedinthewateradditiontreatmentwasassociatedwithcolonizingspeciesineachwateradditionplotbeingmorecloselyrelatedtospeciesinotherreplicateplotsofthesametreatment.Speciescolonizationinthistreatmentwasfoundtobetrait‐based,withleafnitrogenconcentrationbeingthekeyfunctionaltrait.

4. Synthesis.Ouranalysesdemonstratethatanthropogenicenvironmentalchangesmayaffecttheassemblytrajectoriesofplantcommunitiesatbothtaxonomicandphylogeneticscales.Ourresultsalsosuggestthatwhilestochasticprocessesmaycausecommunitiestodivergeinspeciescomposition,deterministicprocesscouldstilldrivecommunitiestoconvergeinphylogeneticcommunitystructure.

K E Y W O R D S

communityassembly,globalchangeecology,nitrogenfertilization,phylogeneticβ‐diversity,precipitationchange,semi‐aridsteppe,taxonomicβ‐diversity

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1  | INTRODUC TION

Understandingmechanisms driving compositional variation acrossecologicalcommunities,frequentlyreferredtoasβ‐diversity,isoneof themajor goals of community ecology (Anderson et al., 2011;Chase&Myers,2011;Whittaker,1960).Acrosslargespatialscales,evolutionaryandbiogeographicprocessessuchas insitudiversifi-cationmayconstituteanimportantsourceofβ‐diversity(Graham&Fine,2008;Ricklefs,2006,2008).Ecological theories thatexplainβ‐diversityamongcommunities,whichgenerallyignoreevolutionaryprocesses,fallintotwobroadcategories.Thenichetheorysuggeststhatβ‐diversity arises largely fromdeterministicprocesses,drivenby ecological selection favouring different species across locali-ties characterizedbydifferent environmental conditions (Chase&Leibold,2003).Incontrast,theneutraltheorysuggeststhatβ-diver-sitycouldsimplyarisefromecologicaldrift,drivenbystochasticpro-cessessuchaschancecolonizationandrandomdemographicevents(Bell, 2001;Hubbell, 2001). Ecological communities are known tobesubjecttotheinfluenceofbothniche‐basedecologicalselection,whichwouldcausecommunitiessharingsimilarenvironmentalcon-ditionstobestructurallysimilar(i.e.lowβ‐diversity),andstochastic-ity‐basedecologicaldrift,whichcouldcausesubstantial structuraldissimilarityamongcommunities (i.e.highβ‐diversity)even insim-ilar environments (Adler,HilleRisLambers,& Levine, 2007;Gravel,Canham,Beaudet,&Messier,2006;Leibold&McPeek,2006).Asanthropogenic environmental changes, such as increasednitrogen(N)depositionandchangingprecipitation,continuetoaffectecosys-temsworld‐wide (Vitousek,Mooney, Lubchenco,&Melillo,1997),it isessential tounderstandhowthesechangesaffecttherelativeimportance of the two contrasting processes in shaping commu-nityassembly,and,consequently,β‐diversityamongtheassembledcommunities.

Anthropogenicenvironmental changes in the formof resourceamendment(e.g.increasedNdepositionandelevatedprecipitation)mayhave thepotential to impact the trajectoryofcommunityas-sembly,andthusβ‐diversity inoppositedirections.Forexampleinenvironmentswherelimitedresourcesupplypresentsanimportantenvironmental filter that excludes many species whose resourcerequirements are not met, increased resource input may relieveenvironmentalharshnessandallowagreaternumberofspeciestosuccessfully colonize thehabitat; the resulting larger species poolcould thenmore readily give rise to alternative community states(Chase, 2003; Fukami, 2004; Jiang, Joshi, Flakes, & Jung, 2011;Law&Morton, 1993; Levine,Bascompte,Adler,&Allesina, 2017;Saavedra et al., 2017), resulting in increased β‐diversity. The in-creased environmental productivity under resource enrichmentmayfurtherpromotethepresenceofalternativecommunitystates(Chase,2010;Ejrnæs,Bruun,&Graae,2006;Isbell,Tilman,Polasky,Binder,&Hawthorne,2013).Ontheotherhand,increasedresourceinputmayfavourspecieswithcertaintraitsbutmaketheconditionlessfavourableforotherspecies(e.g.Dickson,Mittelbach,Reynolds,&Gross, 2014), whichwould lead to increased dominance of thesamespeciesassemblagesacrosscommunities,resultinginreduced

β‐diversity.Inaddition,resourceenrichmentmayoftencausethere-ducedavailabilityofotherresourcesandincreasedintensityofcom-petition for these resources (e.g. light for plants,Hautier,Niklaus,&Hector,2009),acceleratingdeterministiccompetitiveexclusion.

Notably, existing studieson the responseofβ‐diversity toen-vironmental changes have focused on taxonomic β‐diversity thatcapturesturnoverinspeciescompositionamongsites(Chase,2007,2010; Myers, Chase, Crandall, & Jiménez, 2015; Zhang, Liu, Bai,Zhang,&Han,2011). It is less clearhowphylogeneticβ‐diversity,which accounts for evolutionary relationships among species, re-sponds to environmental changes [but seeGuoet al. (2018) for astudyofclimatewarmingonsoilmicrobialcommunities].Studyingphylogeneticβ‐diversity,however,couldprovidenovel insight intohowcommunitiesrespondtoenvironmentalchangesbeyondthoseobtainedviastudyingtaxonomicβ‐diversityalone(Gerhold,Cahill,Winter, Bartish, & Prinzing, 2015; Graham & Fine, 2008; Hardy,Couteron,Munoz,Ramesh,&Pélissier,2012).Forinstancethestudyofbothtaxonomicandphylogeneticβ‐diversitycouldallowtheex-plorationoftheideathatthedegreeofdeterminismincommunityassembly may depend on the level of ecological organization ex-amined(Diamond,1975;Fox,1987;Fukami,Bezemer,Mortimer,&Putten,2005).Agroupofphylogenetically closely related speciesmayexhibitlargelysimilarresponsestoenvironmentalchanges,byvirtueoftheirsimilartraits,makingthegroup‐levelresponsemoredeterministic. However, changes in individual species within thegroupmaybelessdeterministic,astheresultofecologicaldriftin-fluencingpopulationsofcloselyrelatedspecies.Wethushypothe-sizethattaxonomicandphylogeneticβ‐diversitymaynotnecessarilyshowsimilarresponsestoenvironmentalchanges.

Changes in species taxonomic and phylogenetic β‐diversitymay be better understood by looking into species extinction andcolonizationpatterns.Species lossmaydependontheir traitsandevolutionaryhistory,suchthatspeciesofcertaincladesmaysuffergreaterextinctionriskthanspeciesofotherclades(Purvis,Agapow,Gittleman,&Mace,2000).Forexamplelegumes,whichcanwelltol-eratelowsoilNconcentrations,mayexperienceelevatedextinctionunderelevatedNlevels(Stevens,Bunker,Schnitzer,&Carson,2004;Xia &Wan, 2008). The deterministic loss of these clades acrosscommunities,inresponsetoenvironmentalchanges,wouldpromotecommunityconvergence, resulting in reduced taxonomicandphy-logeneticβ‐diversity(Figure1a).Phylogeneticβ‐diversity,however,may not necessarily decline as rapidly as taxonomic β‐diversity ifonlysome,notallspeciesbelongingtothesamecladesfaceextinc-tion. Extinction, however, is far from deterministic (Lande, 1993;Lande,Engen,&Saether,2003).Therandomlossofspecies,espe-ciallythosewithsmallpopulationsizes(Matthies,Bräuer,Maibom,&Tscharntke,2004;Sudingetal.,2005),indifferentlocationsmaydrivedivergenceofspeciescompositionamongcommunities,result-inginincreasedtaxonomicandphylogeneticβ‐diversity(Figure1b,c).Likewise, colonization could be either stochastic or deterministic,causing corresponding changes in taxonomic and phylogenetic β‐diversity(Figure1d,f,g).Colonization‐inducedchangesinphyloge-neticβ‐diversityalsomaynotnecessarilyparallelthoseintaxonomic

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β‐diversity. For example the colonization of a group of species inwhich members are closely related would drive the communitiestowardsphylogeneticconvergence,butmaynotnecessarilycausetaxonomicconvergenceifotherfactors,suchasdispersallimitation,prevent the same species fromcolonizing all localities.Under thiscircumstance,wewouldexpectincreasedtaxonomicβ‐diversitybutdecreasedphylogeneticβ‐diversity(Figure1e).

Here,wereportonafieldexperiment,conductedinatemperatesteppe innorthernChina, to investigate theeffectsofNandpre-cipitationamendmentontaxonomicandphylogeneticβ‐diversityofplant communities. The temperate steppe in this area is currentlyexperiencing significant anthropogenicenvironmental changes, in-cludingincreasedNdepositionandprecipitation(Chenetal.,2013;Niuetal.,2010;Xia,Niu,&Wan,2009),necessitatingathoroughun-derstandingoftheirecologicalconsequences.Previousworkatthestudysitehasdocumentedchangesinanumberofcommunityandecosystemproperties,includingfunctionalgroupcomposition(Yangetal.,2011),ecosystemproductivity,respirationandnetCexchange(Niu et al., 2009, 2010), community stability (Yang et al., 2012)and plant phylogenetic community structure (Yang et al., 2018),in response toexperimentalmanipulationsofNandprecipitation.

However,thequestionofhowtheseenvironmentalchangesaffectthe trajectory of community assembly remains unanswered. WeshowedthatbothNandwateradditionincreasedthestandardef-fective size of taxonomic β‐diversity,whereaswater, notN, addi-tion,reducedthestandardeffectivesizeofphylogeneticβ‐diversity,suggestingthatanthropogenicenvironmentalchangesdifferentiallyaffected plant community assembly trajectories at taxonomic andphylogeneticscales.

2  | MATERIAL S AND METHODS

2.1 | Study site, experimental design and vegetation sampling

TheexperimentwasconductedinanaturalgrasslandattheDuolunRestoration Ecology Station of the Institute of Botany, ChineseAcademy of Sciences, located in a temperate steppe (42o02’ N,116o17’E)inInnerMongolia,China.Thestudyareahasasemi‐aridcontinentalmonsoonclimatewithannualprecipitationof378mmandmeanannualtemperatureof2.1°C.Dominantplantspecies(intermsofcover)inthisareaareperennialgrassesandforbs,including

F I G U R E 1  Aconceptualdiagramofthepotentialeffectsofspeciescolonizationandextinctiononcommunitytaxonomicandphylogeneticbetadiversity.PlotAandBaretworeplicateplotsunderthesameexperimentaltreatments.Forillustrationpurpose,hereweonlyrelatecolonization/extinctioninplotB(focalplot)tocommunitiesinplotA(referenceplot).Theoveralleffectsofspeciescolonizationandextinctiononcommunitytaxonomicandphylogeneticbetadiversitycouldbeassessedbyaveragingallpossiblepairwisecombinationsofreplicateplotsthataresubjecttothesametreatments.Phylogeneticdissimilaritycolonization/extinctinctionisthestandardizedeffectsizeofphylogeneticβ‐diversitybetweencolonized/extinctspeciesinplotBandfinalcommunitycompositionofplotA.(a)ExtinctioneliminatesspeciesinplotBthataredistantlyrelatedtofinalspeciescompositioninplotA,leadingtodecreasedtaxonomicandphylogeneticbetadiversitybetweenthetwoplots.(b)RandomextinctionofspeciesinplotBleadstoincreasedtaxonomicbetadiversityandincreasedorunchangedphylogeneticbetadiversitybetweenthetwoplots.(c)ExtinctioneliminatesspeciesinplotBthatarecloselyrelatedtofinalspeciescompositioninplotA,leadingtoincreasedtaxonomicandphylogeneticbetadiversitybetweenthetwoplots.(d)ColonizationofspeciesintoplotBleadstosimilarfinalspeciescompositioninthetwoplots,leadingtodecreasedtaxonomicandphylogeneticbetadiversitybetweenthetwoplots.(e)ColonizationofspeciesintoplotBthatarenotpresentinplotAbutcloselyrelatedtofinalspeciescompositioninplotAleadstoincreasedtaxonomicbutdecreasedphylogeneticbetadiversitybetweenthetwoplots.(f)RandomcolonizationofspeciesintoplotBleadstoincreasedtaxonomicbetadiversityandincreasedorunchangedphylogeneticbetadiversitybetweenthetwoplots.(g)ColonizationofspeciesthataredistantlyrelatedtofinalspeciescompositioninplotAintoplotBleadstoincreasedtaxonomicandphylogeneticbetadiversitybetweenthetwoplots

(d)

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Stipa krylovii, Artemisia frigida, Potentilla acaulis, Cleistogenes squar-rosa, Allium bidentatum and Agropyron cristatum.Ourstudysitewasheavilygrazedbylivestockpriorto2001; ithasbeenfencedsince2001toexcludelargeherbivores.

Theexperimentused a split‐plot designwithN additionbeingtheprimary factorandwateradditionbeing thesecondary factor.Fourpairsof45×28mplotswereestablished in2005,with twoplotsineachpairassignedtothecontrolandNadditiontreatmentsrespectively.Within each plot,we set up two15× 10m subplotsassignedtothecontrolandwateradditiontreatmentsrespectively.Nenrichmentwasaccomplishedbyadding10gN/m2 year−1 in July 2005intheformofureaandinJulyfrom2006to2013intheformofNH4NO3.TherateofnaturalNdepositioninthestudyareaisap-proximately1.47gN/m2 year−1(Zhangetal.,2017),andtheamountofNadditionappliediscomparabletotherateofatmosphericnitro-gendepositionintheNorthChinaPlain(about8.33gN/m2 year−1; He,Liu,Fangmeier,&Zhang,2007),whereagriculturalactivitiesandfossilfuelconsumptionaremoreconcentrated.Wateradditionwasconductedbyadding15mmofwaterweeklyinJulyandAugust,re-sultinginanapproximately30%increaseinwatersupplyeachyear.Moredetailedinformationonthestudyareaandexperimentalde-signcanbefoundinYangetal.(2012).

Wesurveyedtheexperimentalplots inAugusteachyear from2005 to2013. In eachplot,weplaceda1×1m framewith10010×10cmgridsintoarandomlyselected1×1mquadrat.Allspe-ciesineachgridwereidentifiedandtheircoveragewereestimatedbasedontheiroccurrencewithinthe100grids.Wealsocollecteddata on key plant functional traits, including plant height, rootingdepth,leafNconcentrationandspecificleafarea(SLA).Unlikeourpreviouswork (Yangetal.,2018),whichextractedmost traitdatafromtheTRYdatabase(Kattgeetal.,2011),herewemeasuredmostdata insitu.Plantheightwasmeasuredasthemaximumheightofeachspecies in theexperimentalplotsat thebeginningof theex-periment.Plantsamples for themeasurementofother traitswerecollected fromanearby grasslandoutside theexperimental plots.Rootingdepth,leafNconcentrationandSLAof26commonspeciesweremeasuredaccording toCornelissenetal. (2003).Forspeciesforwhichtraitdatawerenotdirectlymeasured,weextracteddataonrootingdepth,leafNconcentrationandSLAfromtheTRYdata-base(SupportingInformationFigureS1;Kattgeetal.,2011).

2.2 | Phylogenetic tree

Weconstructedaphylogenetictreeforthe52speciesobserved intheexperimentalarea (Supporting InformationFigureS1).First,webuiltagenus‐levelphylogenetictreebasedonthephylogenyofvas-cularplantsgeneratedbyZanneetal.(2014)andQianandJin(2016).However,speciesinthegeneraAllium, Astragalus and Potentilla were absentfromZanneetal.andQian&Jin'sphylogeny.Wethusextractedthe ITS1 and ITS2 sequencesof speciesbelonging to these generafromGenBankandconstructedaphylogenetictreeforeachgenus.WealignedthesequencesfromGenBankwithClustalX(version2.0;Larkin et al., 2007), confirmed the alignment by observation, and

selected thebestevolutionmodelwith jModelTest (version2.1.10;Guindon&Gascuel,2003;Darriba,Taboada,Doallo,&Posada,2012;012,340+G+FforAllium and Potentilla;011,012+FforAstragalus).The phylogeny of each genus was constructed with the Bayesianmethod inMrBayes (version3.1.2;Huelsenbeck&Ronquist,2001),usingtheclosestrelativetoeachgenusastheoutgroup.

2.3 | Species and phylogenetic β‐diversities and their standardized effect sizes

Toassesstreatmenteffectsoncommunityconvergence/divergence,wecalculateddissimilarities inspeciescomposition (i.e. taxonomicβ‐diversity)andphylogeneticstructure(i.e.phylogeneticβ‐diversity)betweenreplicatedplotswithinthesametreatment.Taxonomicβ-diversitywascalculatedusingtheabundance‐weightedBray–Curtisdissimilarity index (Bray&Curtis, 1957). TheBray–Curtis index isrobusttosamplingerrors(Schroeder&Jenkins,2018),andiswidelyused to quantify taxonomic β‐diversity among communities. ThevalueofBray–Curtisdissimilarityapproaches0whenspeciescom-positionisidentical,andapproaches1whenspeciescompositioniscompletelydifferent.Phylogeneticβ‐diversitywasquantifiedusingtheabundance‐weightedpairwisedissimilarityindexDpw(Swenson,2011;Webb,Ackerly,&Kembel,2008).Dpw issuitablefordetect-ingphylogeneticallybasalturnoverbetweencommunitiesandcon-verges to theBray–Curtis dissimilarity index in the case of a starphylogeny(Swenson,2011).Itiscalculatedas:

where k1 and k2aretwocommunities,fiistherelativecoverofspe-cies i in communityk1, fj is the relative coverof species j in com-munityk2, �ik2 isthemeanpairwisephylogeneticdistancebetweenspeciesiincommunityk1andallspeciesincommunityk2excludingconspecificspeciesand�jk1 is themeanpairwisephylogeneticdis-tancebetweenspeciesjincommunityk2andallspeciesincommu-nityk1excludingconspecificspecies.LargervaluesofDpwindicategreaterphylogeneticdistancebetweenthecomparedcommunities.

Inadditiontoniche‐basedandstochasticity‐basedecologicalprocesses,theobservedpatternsoftaxonomicandphylogeneticβ‐diversitymayalsobeaffectedbybothlocalcommunitydiversity(α‐diversity)andthesizeoftheregionalspeciespool(γ‐diversity).Inparticular,whentheregionalspeciespoolremainsunchanged,any factor that changes α‐diversity could potentially alter β-di-versity owing simply to random sampling effects (Anderson etal.,2011;Chase,Kraft,Smith,Vellend,& Inouye,2011;Chase&Myers, 2011;Myers et al., 2013). Therefore,we performed nullmodel analyses to disentangle the variation in β‐diversity fromvariationinα‐diversity.Thenullmodelanalysesdeterminediftheobservedpatternsintaxonomicandphylogeneticβ‐diversitydevi-atedfromtheexpectationsofrandomassembly,afteraccountingfor changes in α‐diversity.Anull distributionof taxonomicβ-di-versitywasgeneratedbyrandomlysamplingindividualsfromthe

(1)Dpw=

∑nk1

i=1fi�ik2 +

∑nk2

j=1fj�jk1

2

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regionalspeciespool999times,whileperseveringthetotalplantcover in each plot and the relative cover of each species in thespeciespool(Kraftetal.,2011).Nulldistributionsofphylogeneticβ‐diversityweregeneratedbyrandomizingthenamesofspeciesacross the tipsof thephylogenetic tree999 times (Webbet al.,2008).Standardizedeffectsize(SES;Gotelli&Graves,1996)wascalculatedfortaxonomic(β‐deviation)andphylogenetic(SES.Dpw)β‐diversityusingthemeanandstandarddeviationoftheirrespec-tivenulldistributions:

where Xobservedistheobservedβ‐diversityvaluebetweentwocom-munities,Xnullisthemeanvalueofthenulldistributionandsd(Xnull)isthestandarddeviationofthenulldistribution.Positiveandneg-ative values indicate higher and lower β‐diversity than expectedbychance,respectively,whereasavalueofzeroindicatesthattheobserved β‐diversitydoesnotdifferfromrandompatterns.

2.4 | Species colonization and extinction

Weclassifiedaspeciestobelocallyextinctfromaplotiftheywerepresent in2005butabsent in2013,anddefinednewcolonistsasspeciesthatwereabsentin2005butpresentin2013inaplot.Toexaminetheeffectofnewcolonistsonthetaxonomicandphyloge-neticdissimilarityamongplotswithinatreatment,wecalculatedtheaverage β‐deviationandphylogeneticSES.Dpwbetweennewcolo-nistsineachreplicateplotandfinalspeciescompositioninthethreeotherreplicateplotsunderthesametreatment(β‐deviation(C)andSES.Dpw(C)).Anegativeβ‐deviation(C)orSES.Dpw(C)indicatesthatnew colonists in a plot aremore similar or phylogeneticallymorecloselyrelatedtothespeciescompositioninotherplotsofthesametreatmentsthanexpectedbychancerespectively.Toexaminetheeffect of the extinct species on the taxonomic and phylogeneticdissimilarityamongplotswithinatreatment,wecalculatedtheav-erage β‐deviationandphylogeneticSES.Dpwbetweenextinctspe-ciesineachreplicateplotandthefinalspeciescompositionintheotherreplicateplotsunderthesametreatment(β‐deviation(E)andSES.Dpw(E)).Forspeciesextinction,apositiveβ‐deviation(E)orSES.Dpw(E)indicatesthattheextinctspeciesinaplotaremoredissimilarorphylogeneticallymoredistantlyrelatedtotheremainingspeciesinotherplotsofthesametreatmentsthanexpectedbychancere-spectively.Toaddressthepossibilitythattheresultsbasedon2005and2013onlymaybevulnerabletoobservationerror,wealsodi-vided the experiment into three periods (2005–2007, 2007–2010and2010–2013), andanalysedβ‐deviation(C/E) andSES.Dpw(C/E)foreachperiod.Consistentresultsbetweenthethreeperiodswouldlendgreatercredibilitytoourresults.

Toassess thecontributionsof species’ functional traitson thepatternofSES.Dpw,wecalculatedSES.Dpwvaluesoffunctionaltraitsforbothcolonistandextinctspeciesusingthedendrogramsofthemeasured functional traits (i.e. plant height, rooting depth, leafN

concentrationandSLA).Wegeneratedfourtraitdendrograms,onefor each functional trait, using UPGMA clustering based on theEuclideandistancematrix(Petchey&Gaston,2002).

2.5 | Statistical analysis

To test for theeffectsofNandwateradditionon taxonomicandphylogenetic β‐diversity and their standardized effect sizes overtime, we conducted a permutational multivariate analysis of vari-ance (PERMANOVA;999permutations;Anderson,2001) inwhichfertilization, watering, time and their interactions were used asexplanatory variables. FollowingPERMANOVA,we also usedper-mutationalanalysisofmultivariatedispersions (PERMDISP) totestwhethercommunitiesdifferintheirwithin‐treatmentdissimilarities(Anderson,2006;Anderson,Ellingsen,&McArdle,2006).

We calculated the phylogenetic signal of the four functionaltraits measured in this study using the K statistic (Blomberg,Garland,& Ives, 2003). The significance (p‐values) of thephylo-genetic signalwasevaluatedbycomparing thevarianceof inde-pendentcontrastsforeachtraittotheexpectedvaluesobtainedbyshufflingleaftraitdataacrossthetipsofthephylogenetictree999 times. To assess the importance of species’ initial coverageandfunctionaltraitsoncolonizationandextinction,weranlogis-ticregressionsofspeciescolonization/extinctionasafunctionofspecies’initialcoverageandtraitvalues(i.e.plantheight,rootingdepth,leafNconcentrationandSLA).Speciesthatdidnotcolonizeorgoextinctinanyplotwithinatreatmentwereassignedavalueof0.Otherwise,specieswereassignedavalueof1.Weassignedvaluesforcolonizationandextinctionseparately.

AllanalyseswereperformedusingR3.5.1(RCoreTeam.,2018).TheBray–Curtis indexwascalculatedusingthevegdist functioninthepackagevegan (Oksanenet al., 2018), andDpwwascalculatedusing the comdist function in the package picante (Kembel et al.,2010). The null communities were generated using the nullmodel in the vegan package (Oksanen et al., 2018). PERMANOVA andPERMDISPwereperformedusing the functionsadonis2 and beta-disper in the veganpackagerespectively(Oksanenetal.,2018).TheanalysesonphylogeneticsignalwereconductedusingthefunctionmultiPhylosignalinthepicantepackage(Kembeletal.,2010).

3  | RESULTS

3.1 | Species taxonomic and phylogenetic β‐diversity, and their standardized effect size

Taxonomic β‐diversity (Bray–Curtis index) fluctuated significantlyovertimeinallbutthewateradditiontreatments.Taxonomicβ-di-versityexhibitedapositivetrendonlyintheNadditiontreatment,resulting in greaterβ‐diversity in this treatment than the controls(Figure 2a). Phylogenetic β‐diversity (Dpw) remained largely un-changed intheNadditionandN+wateradditiontreatments,butdeclinedovertimeinthecontrolandwateradditionplots,resultingingreaterphylogeneticβ‐diversityintheNadditionandN+water

(2)SES.X=Xobsered−Xnull

sd(

Xnull)

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addition plots towards the end of the experiment (Figure 2c).PERMANOVAindicatedthatNenrichment,wateraddition,yearandalltheirtwo‐wayinteractiontermssignificantlyaffectedtaxonomicβ‐diversity,whereasphylogeneticβ‐diversitywasonlysignificantlyaffectedbyNaddition(Table1).PERMDISPrevealedthatN,waterandN+wateradditiontreatmentincreasedthedispersionofspe-ciescomposition(SupportingInformationFigureS2).

β‐deviation showed a similar temporal pattern as the Bray–Curtisindex.Attheendoftheexperiment,β‐deviationwasnotsig-nificantly different fromnull expectation in the control plots, butwas significantlyhigher thannull expectation in theN,water andN+wateradditiontreatments,withthehighestvaluesobservedfortheNadditionplots(Figure2b).ThestandardizedeffectsizeofDpw (i.e.SES.Dpw)wassignificantlygreaterthanzeroinalltreatmentsini-tially(one‐samplet‐test,p<.05).Attheendoftheexperiment,how-ever,SES.Dpwwassignificantlynegative(one‐samplet‐test,p=.018)in the water addition plots and not significantly different fromzerointheothertreatments(one‐samplet‐test,p>.05;Figure2d).

Correspondingly,PERMANOVAindicatedthatNenrichment,wateradditionand their interaction termssignificantlyaffectedβ-devia-tionandthatSES.Dpwwasonlyaffectedbywateraddition(Table1).PERMDISP revealed thatDpwshowedgreaterdispersion in theN,waterandN+wateradditiontreatmentsthanthecontrols,whereasSES.Dpwshowedlowerdispersioninthewateradditiontreatmentthanothertreatments(FigureS2,TableS1).

3.2 | Species colonization and extinction

Inthecontrolplots,mostoftheextinctspecieswereforbsfromthegenera Allium and Potentilla andmostcolonistsweregrasses fromthefamilyPoaceae.InplotswithNfertilization,inadditiontospe-ciesthatwentextinctinthecontrols,somegrassesfromthefamilyPoaceaeandCyperaceaealsowentextinct;thefewcolonistsweremainlyforbsfromthefamiliesRosaceaeandCruciferae.Inthewateraddition plots, however, the number of extinct specieswasmuchlower, with most being extinct also in the control plots. Species

F I G U R E 2  Changesintaxonomicβ‐diversity,phylogeneticβ‐diversityandtheirrespectivestandardizedeffectsizesamongreplicateplotswithineachtreatmentovertime.Taxonomicβ‐diversityanditsstandardizedeffectsizeweremeasuredby(a)Bray–Curtisdissimilarityand(b)β‐deviationrespectively.Phylogeneticβ‐diversityanditsstandardizedeffectsizeweremeasuredby(c)Dpwand(d)SES.Dpw respectively.Valuesaremean±standarderror.Thestandardizedeffectsizes(β‐deviationandSES.Dpw)showthemagnitudeofdeviationbetweenobservedβ‐diversityandthevaluesgeneratedfromnullmodels.Negativevaluesindicatelowerβ‐diversitythanexpectedfromchance,whereaspositivevaluesindicatetheopposite

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F p F p F p F p

N 1 20.45 .001 11.62 .001 1.79 .001 0.87 1.000

Water 1 5.21 .001 1.17 0.181 1.15 .001 1.02 .035

Year 1 12.42 .001 1.55 0.055 1.00 .467 0.98 .924

N:W 1 2.69 .016 1.10 0.212 1.08 .032 0.99 .858

N:Y 1 3.69 .002 1.63 0.047 1.16 .003 1.00 .614

W:Y 1 2.66 .011 1.30 0.113 1.10 .012 1.01 .110

N:W:Y 1 1.02 .382 0.92 0.499 1.00 .500 0.99 .765

TA B L E 1  Resultsofpermutationalmultivariateanalysisofvariance(PERMANOVA)ontheeffectsofNenrichment,wateraddition,yearandtheirinteractionsoncommunitytaxonomicβ‐diversity(Bray–Curtis),phylogeneticβ‐diversity(Dpw)andtheirrespectivestandardeffectsizes(β‐deviationandSES.Dpw).Theanalyseswereperformedusing999permutations.p < 0.05 shown in bold.

     |  2127Journal of EcologyYANG et Al.

colonizingthewateradditionplotsweremainlyforbsfromthefami-liesLabiatae,GentianaceaeandLeguminosae(FigureS1).

The compositional dissimilarity between colonists and finalcommunitycompositionwithinatreatment(i.e.β‐deviation(C))wassignificantlygreaterthanzeroinalltreatments,indicatingthatcol-onistsweremoredissimilartospeciesinotherreplicateplotsthannull expectation (Figure 3a; one‐sample t‐test,p < .05). The com-positionaldissimilaritybetweenextinctspeciesandthe finalcom-munitycompositionwithinatreatment(i.e.β‐deviation(E))wasalsosignificantlygreaterthanzeroinalltreatments(Figure3b;one‐sam-plet‐test,p<.05),indicatingtaxonomicallydeterministicextinction.ThephylogeneticSES.Dpwbetweencolonistsand finalcommunitycompositionwithinatreatment(i.e.SES.Dpw(C))didnotsignificantlydiffer fromzero in thecontrol,NadditionandN+wateradditiontreatments (Figure 3c; one‐sample t‐test,p > .05), indicating phy-logenetic randomnessof speciescolonization in these treatments.However,wefoundsignificantnegativephylogeneticSES.Dpw(C)inthewateradditiontreatment(Figure3c;one‐samplet‐test,p=.035),indicatingthatcolonizingspecies ineachwateradditionplotweremorecloselyrelatedtospeciesinotherreplicateplotsthanexpectedbychance.ThephylogeneticSES.Dpwbetweenextinctspeciesandfinal community compositionwithin a treatment (SES.Dpw(E)) wasnotsignificantlydifferentfromzerointheN,waterandN+wateradditiontreatments(Figure3d;one‐samplet‐test,p>.05),indicatingphylogeneticrandomnessofspeciesextinctioninthesetreatments.The average phylogenetic SES.Dpw(E) in the controls was signifi-cantly greater than zero (Figure 3d; one‐sample t‐test, p = .011),

indicating thatextinctionexcluded species thatweremorephylo-genetically distantly related to the final species composition thanexpectedbychanceinthistreatment.Whentheexperimentwasdi-videdintothreeperiods(2005–2007,2007–2010and2010–2013),thepatternsforβ‐deviation(C/E)andSES.Dpw(C/E)withineachpe-riodweresimilartothoseacrossallyears(FigureS3).

Amongthefourfunctionaltraitsmeasuredinthisstudy,signifi-cantphylogeneticsignalwasdetectedonlyforleafNconcentration(p= .035,TableS1).Therefore,wepresentedtheresultsonleafNconcentration inthemaintextandtheresultsonother functionaltraitsinthesupportinginformation(SupportingInformationFigureS4, S5, Appendix A, B). The SES.Dpw(C) for leaf N concentrationshowed a similar patternwith phylogenetic SES.Dpw(C), such thatcolonizingspeciesineachwateradditionplotweremoresimilarinleafNconcentrationwithspecies inother replicateplots thanex-pectedbychance(Figure4a,one‐samplet‐test,p=.036).Forspeciesextinction,non‐significantSES.Dpw(E)forleafNconcentrationwasfoundforalltreatments(Figure4b).

Theinitialcoverageofspecieswasasignificantpredictorofspe-ciesextinctioninalltreatments.Specieswithlowerinitialcoveragetendedtohaveagreaterprobabilityofextinction(Figure5a–d),cor-respondingwiththetaxonomicallydeterministicextinctionfoundinall treatments (showninFigure3b).LeafNconcentrationaffectedthe likelihood of species colonization in thewater addition treat-ment,suchthatspecieswithhigherleafNconcentrationsweremorelikely tocolonize (Figure5g). In theN+wateradditiontreatment,leafNconcentrationaffected the likelihoodof speciesextinction,

F I G U R E 3  Thetaxonomic(β‐deviation)andphylogeneticdissimilarity(SES.Dpw)between(a,c)newcolonistsand(b,d)extinctspeciesofeachplotandfinalspeciescompositionintheotherthreereplicateplotswithinthesametreatment.Forspeciescolonization,anegativeβ‐deviation(C)indicatesthatnewcolonistsaremoresimilartothefinalcommunitiesinotherreplicatesthanexpectedbychance,andanegativeSES.Dpw(C)indicatesthatnewcolonistsaremorephylogeneticallycloselyrelatedtothefinalcommunitiesinotherreplicatesthanexpectedbychance,indicatingdeterministiccolonization.Forspeciesextinction,apositiveβ‐deviation(E)indicatesthatextinctspeciesaremoredissimilartotheremainingspeciesinotherreplicatesthanexpectedbychance,andSES.Dpw(E)indicatesthatextinctspeciesaremorephylogeneticallydistantlyrelatedtotheremainingspeciesinotherreplicatesthanexpectedbychance,indicatingdeterministicextinction. *denotesvaluesthataresignificantlydifferentfromzerobasedonone‐samplettest(p<.05).Errorbarsrepresentstandarderrors

0

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Colonization Extinction(a) (b)

(c) (d)

2128  |    Journal of Ecology YANG et Al.

suchthatspecieswithhigherNconcentrationsufferedfromgreaterriskofextinction(Figure5h).

4  | DISCUSSION

The Earth's ecosystems are facing widespread anthropogenic en-vironmental changes. A key challenge is to elucidate how ecologi-cal processes interact with evolutionary processes in influencingdiversitypatternsacrossspatialscalesinthefaceofanthropogenicenvironmental changes. In this study, we investigated the impactof elevated N deposition and precipitation on species taxonomicand phylogenetic β‐diversity, and linked species colonization and

extinctiontotheobservedβ‐diversitypatterns.WefoundthatbothNenrichmentandwateradditionsignificantlyincreasedtaxonomicβ-diversity,andNenrichmentalsosignificantlyincreasedphylogeneticβ‐diversity.However,whenthedifferences in localcommunitysizewerecontrolledforusingnullmodels,bothNenrichmentandwateradditionsignificantlyincreasedthestandardeffectsizeoftaxonomicβ‐diversity(i.e.β‐deviation),suggestingthatresourceenrichmentledto increased taxonomic divergence; water addition, not N enrich-ment,significantlydecreasedthestandardeffectsizeofphylogeneticβ‐diversity(i.e.SES.Dpw),suggestingthatwateradditiondrovecom-munitiestoconvergetowardsmoresimilarphylogeneticstructure.

A number of experiments have assessed the effects of re-source addition on taxonomicβ‐diversity. Chalcraft et al. (2008)

F I G U R E 4  Thefunctionaltraitdissimilarity(SES.Dpw)forleafNconcentrationbetweennewcolonists(a)andextinctspecies(b)ofeachplotandfinalspeciescompositionintheotherthreereplicateplotswithinthesametreatment.AnegativeSES.Dpw(C)indicatesthatnewcolonistsaremoresimilartothefinalspeciescompositionthanexpectedbychance.ApositiveSES.Dpw(E)indicatesthatextinctspeciesaremoredifferentfromtheremainingspeciesthanexpectedbychance.*denotesvaluesthataresignificantlydifferentfromzerobasedonone‐samplettest(p<.05).Errorbarsrepresentstandarderrors

–1.0

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F I G U R E 5  Speciescolonization(blackcircles)andlocalextinction(redcircles)asfunctionsofinitialcoverage(a–d)andleafNconcentration(e–h)ineachtreatment.Speciesthatdidnotcolonizeorgoextinctinanyplotwithinatreatmentwasassignedavalueof0.Otherwise,specieswereassignedavalueof1.Significantlogisticregressionlines(p<.1)areshown

(a) (b) (c) (d)

(e) (f) (g) (h)

     |  2129Journal of EcologyYANG et Al.

synthesizeddatafrom18N‐enrichmentexperimentsalongapro-ductivitygradientacrossNorthAmerica,andfoundthatNadditionpromoted β‐diversity at low‐productivity sites but reduced β-di-versityathigh‐productivitysites,withthethresholdproductivityaround 400 g m−2 year−1.Thepositivetreatmenteffectsonβ-di-versityinourexperimentareinaccordancewiththisgeneralpat-tern,astheproductivityatourstudysiteisfarbelowthethreshold(60~250gm−2 year−1,Xuet al., 2018).Nandwater areknownto be the two major limiting resources for our study grassland(Bai,Han,Wu,Chen,&Li,2004;Niuetal.,2010).Ourresultsarethus consistent with the idea that adding limiting resources en-hances β‐diversityinresource‐scarceenvironments,wherestrongenvironmentalfilteringlimitscommunitymembershipinalargelydeterministicmanner (Chalcraft et al., 2008;Chase, 2010).Notethat in our experiment, both taxonomic β‐diversity and β-devia-tionincreasedinresponsetoNandwateraddition,indicatingthatthe observed community divergence afterN andwater additionwasduetotheenhancedroleofstochasticprocessesratherthanchanges in α‐diversity.Onepossiblemechanismforthemoreim-portantroleofstochasticassemblyprocessesunderresourceen-richmentisthatstrongerpriorityeffectsmayleadtotheincreasedlikelihoodofmultiple community states inmorebenignenviron-ments(Chase,2003,2007,2010).Inourstudy,dispersalwashighlystochasticatthespecieslevel,asevidencedbythecompositionaldissimilaritybetweencolonizedspeciesineachplotandspeciesinother replicateplots (i.e.β‐deviation (C))beingmuchhigher thannull expectation in all treatments. Under resource amendment,suchstochasticdispersalmayhaveledtohighvariabilityinspeciesarrivalhistoryand, inturn,strongpriorityeffects,promotingthetaxonomic divergenceof communities (Chase, 2010;Vannette&Fukami,2017).

Wefoundthatwateraddition,ratherthanNenrichment,signifi-cantlydecreased the standardeffect sizeofphylogeneticβ-diver-sity(SES.Dpw),drivingthecommunitiesfrombeingphylogeneticallydivergent to being phylogenetically convergent (Figure 2d). Suchtransitioninthewateradditiontreatmentcouldbeattributedtothephylogenetically non‐random colonization of species. Specifically,thecolonistsineachplotafterwateradditionweresignificantlyre-latedtospeciesinotherreplicateplots(Figure3c),resultinginphylo-geneticallysimilarcommunitycompositionamongplots.Thispatterncontrastswiththetaxonomicallystochasticcolonizationanddiver-genceobservedinthewateradditionplots(seethepreviouspara-graph),supportingourhypothesisthattaxonomicandphylogeneticβ‐diversitymaynotnecessarilyrespondsimilarlytoenvironmentalchanges (Graham&Fine,2008;Hardyet al., 2012).These resultsemerged likely becausewater addition favours certain closely re-latedspecieswithsimilartraits(e.g.thosewithsimilarleafNcontent,Figure4a),resultingincommunityconvergenceatthephylogeneticscale,butfacilitatesthenon‐deterministiccolonizationofthesespe-ciesamongplots (Figure3a),resulting incommunitydivergenceatthespecieslevel.Onewaytoconfirmthisexplanationistoeliminatethestochasticityassociatedwithspeciescolonizationby,forexam-ple seedaddition,whichwould favourcommunityconvergenceat

bothtaxonomicandphylogeneticscales.Indeed,arecentstudyhasfoundthatfertilizationandwateradditionintoaCaliforniagrasslandreducedplanttaxonomicβ‐diversitywhenseedsofcommonspecieswereaddedtoallexperimentalplots(Eskelinen&Harrison,2015).On theotherhand,our resultsclearlyshowthatconsideringbothphylogeneticandtaxonomicturnoverallowsabetterassessmentoftheroleofdeterministicandstochasticprocessesinshapingecolog-icalcommunities.

We foundevidence for functional trait‐based species coloni-zationinthewateradditionplots.LeafNconcentration,theonlyplanttraitthatexhibitedsignificantphylogeneticsignal(TableS2),was found tobemore similar between the colonist in eachplotandthespeciesinotherreplicateplotsinthewateraddition,butnotothertreatments(Figure4a).Correspondingly,theprobabilityofcolonizationwasstronglyassociatedwithleafNconcentration,withN‐richspeciestendingtohaveagreaterprobabilityofcoloni-zation(Figure5g).LeafNconcentrationisakeyfunctionaltraitonthe“leafeconomicspectrum”that relatestoplant resourcecap-ture and conservation (Wright et al., 2004). N‐poor species aregenerally conservative in resource use and expected to be bet-ter at copingwithabiotic stress (Coley,Bryant,&Chapin,1985;Díazetal.,2016;Reich,Walters,&Ellsworth,1997;Wrightetal.,2004).Studiesthatexploredrelationshipsbetweenleafeconomictraits andclimatehave foundageneral tendency for species in-habitingaridandsemi‐aridregionstoexhibitamoreconservativestrategyinresourceuse(Wright,Reich,&Westoby,2001).Inlinewiththesefindings,ourresultdemonstratedthatenhancedwatersupplyalleviatedabioticstressandfacilitatedspeciesonthe“ac-quisitive” end of the leaf economic spectrum to colonize,whichresulted in phylogenetic homogenization among water additionplots. Finally,wenote that traits of the sameplant speciesmayrespond to resource amendment, such that theymay alsodifferamongexperimentaltreatments(Yanetal.,2015).Thispossibility,however,wouldneedtobeaddressedbyfuturestudies,asweonlyquantifiedplanttraitsinthecontrols.

Our study provides, to our knowledge, the first experimen-tal evidence that anthropogenic environmental changes can dif-ferentially affect plant taxonomic and phylogenetic β‐diversity.Both N enrichment and water addition significantly increasedtaxonomicβ‐diversity,whereaswateraddition,notNenrichment,significantly reducedphylogeneticβ‐diversity,with the latterat-tributed to colonizing species in eachwater addition plot beingmorecloselyrelatedtospeciesinotherreplicateplotsofthesametreatment.Ourresultsthusillustratethatalthoughstochasticpro-cessesmaycausecommunitiestodivergemoreinspeciescompo-sitionunderanthropogenicenvironmentalchanges,deterministicprocesses could still produce communities more convergent inphylogeneticcommunitystructure.Itremainstobeseenwhetherthesefindingsapplytoothersystemsandwhethertheyextendtoecosystemfunctions.Forexamplean interestingquestiontoasknextiswhethercommunityphylogeneticconvergenceunderpre-cipitationamendmentwould translate intoecosystemfunctionalconvergence.

2130  |    Journal of Ecology YANG et Al.

ACKNOWLEDG EMENTS

This project was supported by the National Natural ScienceFoundation of China (grant no. 31361123001, 31430015 and31770522)andtheNationalScienceFoundationofUSA(grantno.DEB‐1342754,DEB‐1856318 andCBET‐1833988).Wedeclare noconflictofinterest.

AUTHORS’ CONTRIBUTIONS

S.W.,L.J.andX.Y.conceivedtheproject;G.L,D.S.,H.S.,M.Z.,Z.Z.,J.S. and J.R. carriedout the field experiments and collecteddata;X.Y.analysedthedata;X.Y.andL.J.wrotethefirstdraftofthemanu-script;allauthorscontributedsubstantiallytorevisions.

DATA AVAIL ABILIT Y S TATEMENT

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.nh1s3k3(Yangetal.,2019).

ORCID

Xian Yang https://orcid.org/0000‐0002‐1527‐7673

Guoyong Li https://orcid.org/0000‐0003‐0932‐4063

Mingxing Zhong https://orcid.org/0000‐0003‐0397‐3863

Jian Song https://orcid.org/0000‐0001‐9957‐6533

Lin Jiang https://orcid.org/0000‐0002‐7114‐0794

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How to cite this article:YangX,LiG,LiS,etal.Resourceadditiondrivestaxonomicdivergenceandphylogeneticconvergenceofplantcommunities.J Ecol. 2019;107:2121–2132. https://doi.org/10.1111/1365‐2745.13253